Differential control and function of Arabidopsis ProDH1 and ProDH2 genes on infection with biotrophic and necrotrophic pathogens

Mol Plant Pathol. 2017 Oct;18(8):1164-1174. doi: 10.1111/mpp.12470. Epub 2016 Oct 17.

Abstract

Arabidopsis contains two proline dehydrogenase (ProDH) genes, ProDH1 and ProDH2, encoding for homologous and functional isoenzymes. Although ProDH1 has been studied extensively, especially under abiotic stress, ProDH2 has only started to be analysed in recent years. These genes display distinctive expression patterns and show weak transcriptional co-regulation, but are both activated in pathogen-infected tissues. We have demonstrated previously that Arabidopsis plants with silenced ProDH1/2 expression fail to trigger defences against the hemibiotrophic bacterial pathogen Pseudomonas syringae pv. tomato AvrRpm1 (Pst-AvrRpm1), and that ProDH1 and ProDH2 are differentially regulated by salicylic acid (SA). In the current work, we used prodh1 and prodh2 single-mutant plants to assess the particular contribution of each gene to resistance against Pst-AvrRpm1 and the necrotrophic fungal pathogen Botrytis cinerea. In addition, we studied the sensitivity of ProDH1 and ProDH2 to the jasmonic acid (JA) defence pathway. We found that ProDH1 and ProDH2 are both necessary to achieve maximum resistance against Pst-AvrRpm1 and B. cinerea. However, ProDH2 has a major effect on early restriction of B. cinerea growth. Interestingly, ProDH1 is up-regulated by SA and JA, whereas ProDH2 is only activated by JA, and both genes display transcriptional inter-regulation at basal and infection conditions. These studies provide the first evidence of the contribution of ProDH2 to disease resistance, and describe the differential regulation and non-redundant but complementary function of both enzyme isoforms in infected tissues, providing support for a fundamental role of ProDH in the control of biotrophic and necrotrophic pathogens.

Keywords: B. cinerea; HopX1; Pst-AvrRpm1; jasmonate; prodh1-3 and prodh2-2; proline dehydrogenase; salicylic acid.

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / genetics*
  • Arabidopsis / microbiology*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Botrytis / pathogenicity*
  • Cyclopentanes / pharmacology
  • Gene Expression Regulation, Plant / drug effects
  • Genes, Plant*
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism
  • Mutation / genetics
  • Oxylipins / pharmacology
  • Plant Diseases / genetics
  • Plant Diseases / microbiology*
  • Proline Oxidase / genetics*
  • Proline Oxidase / metabolism
  • Pseudomonas syringae / pathogenicity*
  • Salicylic Acid / pharmacology

Substances

  • Arabidopsis Proteins
  • Cyclopentanes
  • Mitochondrial Proteins
  • Oxylipins
  • jasmonic acid
  • PDH1 protein, Arabidopsis
  • Proline Oxidase
  • ProDH2 protein, Arabidopsis
  • Salicylic Acid